*3.2.2. Fish prey*

OC pesticides, including ∑DDTs, chlordanes, *β*-HCH, dieldrin and mirex, and individual PCB congeners detected in Galapagos sea lion pups were also detected (> MDL) in all sampled thread herring and mullet prey samples. Significantly lower concentrations of OC pesticides and PCBs were found in thread herrings and mullets than in Galapagos sea lion pups (ANOVA and multi-comparisons Tukey-Kramer (HSD) post-hoc test, *p*< 0.05; Table 1). PCB 202 was the only congener exhibiting similar concentrations in sea lions and fish (ANOVA, *p*> 0.05), suggesting a lack of its bioaccumulation in the food chain. Although thread herring and mullet showed differences in *δ*15*N* values or trophic levels and foraging strategies, concentrations of POPs in these two species were similar (Figure 2) with the exception of mirex and *cis*-nonachlor, which were higher in planktivorous thread herrings than in mullets. Endosulfan sulphate was detected in all mullet samples ranging from 0.07 to 0.22 *μ*g/kg lipid, with an arithmetic mean of 0.16 *μ*g/kg lipid. Only two thread herring samples exhibited detectable concentration of this pesticide (0.002–0.05 *μ*g/kg lipid). Endosulfan sulphate was not detected in any of the biopsy samples of pups.

Assessing Biomagnification and Trophic Transport of Persistent Organic Pollutants in the Food Chain of the Galapagos Sea Lion (*Zalophus wollebaeki*): Conservation and Management Implications 89

*p***-value** 

**Galapagos sea lion (predator) Fish (prey)**

 (*n* = 10) (*n* = 10) (*n* = 4) (*n* = 6) **Lipid (%)** 75.9 ± 3.50 77.8 ± 2.45 1.22 ± 0.86 2.86 ± 2.00

**Female pups Male pups Thread herring Mullet**

*p***,***p***'-DDE** 480 ± 120 **A** 505 ± 180 **A** 3.30 ± 1.00 **B** 2.22 ± 0.700 **B** <0.05\*

*p***,***p***'-DDT** 13.0 ± 2.85 **A** 8.60 ± 1.08 **A** 0.070 ± 0.046 **B** 0.130 ± 0.051 **B** <0.05\* (1.70–29.0) (0.974–12.0) (ND–0.195) ND–0.300 *p***,***p***'-DDD** 20.0 ± 4.73 **A** 17.0 ± 4.60 **A** 0.440 ± 0.140 **B** 0.550 ± 0.170 **B** <0.05\*

**∑DDT** 516 ± 125 **A** 533 ± 183 **A** 4.00 ± 1.26 **B** 3.00 ± 0.910 **B** <0.05\*

**Mirex** 8.60 ± 1.76 **A** 6.40 ± 2.20 **A** 0.330 ± 0.030 **B** 0.040 ± 0.008 **C** <0.05\*\*

**Dieldrin** 31.0 ± 7.26 **A** 22.0 ± 4.80 **A** 0.600 ± 0.204 **B** 0.880 ± 0.128 **B** <0.05\*\*

*β***-HCH** 34.2 ± 4.00 **A** 26.0 ±7.05 **A** 0.440 ± 0.090 **B** 0.495 ± 0.095 **B** <0.05\*\*

**chlordane** 0.410 ± 0.100 **<sup>A</sup>** 0.65 ± 0.10 **A** 0.070 ± 0.027 **B** 0.040 ± 0.015 **<sup>B</sup>** <0.05\*\*

**chlordane** 17.2 ± 2.67 **A** 15.0 ± 2.75 **A** 0.455 ± 0.140 **B** 0.250 ± 0.053 **<sup>B</sup>** <0.05\*

**nonachlor** 73.0 ± 12.0 **A** 65.0 ± 22.0 **A** 0.860 ± 0.191 **B** 0.40 ± 0.072 **<sup>B</sup>** <0.05\*\*

**nonachlor** 16.0 ± 3.20 **A** 10.0 ± 2.10 **A** 0.300 ± 0.109 **B** 0.195 ± 0.050 **<sup>C</sup>** <0.05\*

**∑Chlordanes** 107 ±15.0 **A** 90.5 ± 25.2 **A** 1.70 ± 0.445 **B** 0.870 ± 0.175 **B** <0.05\*

**PCB 52** 3.20 ± 0.530 **A** 2.10 ± 0.610 **A** 0.210 ± 0.030 **B** 2.20 ± 1.85 **B** <0.05\*\* (1.13–5.60) (0.332–7.05) (0.136–0.270) (0.055–11.0) **PCB 74** 2.60 ± 0.410 **A** 2.00 ± 0.510 **A** 0.100 ± 0.009 **B** 0.280 ± 0.220 **B** <0.05\*\*

**PCB-95** 2.80 ± 0.303 **A** 2.20 ± 0.320 **A** 0.300 ± 0.090 **B** 2.02 ± 1.70 **B** 0.05\*\*

(48.1–180) (18.8–255) (0.481–2.50) (0.372–1.50)

*trans***-**

*cis***-**

*trans***-**

*cis***-**

(65.4–1183) (13.6–1650) (0.669–5.00) (0.620–5.20)

(1.88–44.0) (0.965–54.0) (0.036–0.70) (0.155–1.30)

(71.2–1230) (16.3–1666) (0.705–6.05) (0.820–6.80)

(2.50–21.0) (0.850–24.0) (0.250–0.400) (0.028–0.080)

(9.00–83.0) (9.00–63.0) (0.005–0.90) (0.400–1.30)

(18.3–52.0) (7.75–78.0) (0.229–0.620) (0.041–0.650)

(ND–0.840) (0.273–1.03) (ND–0.130) (ND–0.110)

(6.800–34.0) (3.60–31.0) (0.049–0.670) (0.120–0.482)

(37.0–146) (11.0–214) (0.430–1.30) (0.160–0.570)

(3.7–31.8) (3.56–25.8) (ND–0.510) (0.075–0.380)

(1.40–5.10) (0.340–4.40) (0.050–0.085) (0.012–1.40)

(1.63–4.83) (0.873–3.75) (0.018–0.413) (0.026–10.4)

**Figure 2.** Inter-species comparisons of ∑PCB and organochlorine pesticide (mirex, dieldrin, *β*-HCH, ∑Chlordanes, *p*,*p*-DDE, ∑DDT) concentrations. Asterisks indicate that concentration in the Galapagos sea lion were significantly higher (p < 0.05) than those found in mullets and thread herrings. Error bars are standard deviations.

The PCB composition in prey showed a different composition of PCB congeners compared to that of sea lions pups (Figure 3). Higher chlorinated PCBs, i.e., Hepta, Octa and Nonachlorinated biphenyls (PCBs 180–201) were more abundant in thread herrings and mullets than in Galapagos sea lion pups. This indicates the possible role of biotransformation, reduced uptake of PCBs, or a natural placental barrier for heavier PCBs in sea lions. Lower chlorinated PCB congeners, ranging from PCB 43/44 to PCB 118 (Tetra to Penta- chlorinated biphenyls), make up an important contribution (≈ 37% ± 7.25%) to the total PCB concentrations suggesting a lighter PCB signature ("equatorial fingerprint") in the Galapagos sea lion, mullet and thread herring compared to that observed in many arctic biota.


Assessing Biomagnification and Trophic Transport of Persistent Organic Pollutants in the Food Chain of the Galapagos Sea Lion (*Zalophus wollebaeki*): Conservation and Management Implications 89

88 New Approaches to the Study of Marine Mammals

biopsy samples of pups.

**-2.00 -1.50 -1.00 -0.50 0.00 0.50 1.00 1.50 2.00 2.50 3.00 3.50**

biota.

are standard deviations.

**Log POPs (μg/kg lipid)**

fish (ANOVA, *p*> 0.05), suggesting a lack of its bioaccumulation in the food chain. Although thread herring and mullet showed differences in *δ*15*N* values or trophic levels and foraging strategies, concentrations of POPs in these two species were similar (Figure 2) with the exception of mirex and *cis*-nonachlor, which were higher in planktivorous thread herrings than in mullets. Endosulfan sulphate was detected in all mullet samples ranging from 0.07 to 0.22 *μ*g/kg lipid, with an arithmetic mean of 0.16 *μ*g/kg lipid. Only two thread herring samples exhibited detectable concentration of this pesticide (0.002–0.05 *μ*g/kg lipid). Endosulfan sulphate was not detected in any of the

**mirex dieldrin β-HCH ∑Chlordanes ∑PCB p,p'-DDE ∑DDT**

**\***

**\***

**\***

**\***

**\***

**Mullet Thread herring Galapagos sea lion**

**Figure 2.** Inter-species comparisons of ∑PCB and organochlorine pesticide (mirex, dieldrin, *β*-HCH, ∑Chlordanes, *p*,*p*-DDE, ∑DDT) concentrations. Asterisks indicate that concentration in the Galapagos sea lion were significantly higher (p < 0.05) than those found in mullets and thread herrings. Error bars

The PCB composition in prey showed a different composition of PCB congeners compared to that of sea lions pups (Figure 3). Higher chlorinated PCBs, i.e., Hepta, Octa and Nonachlorinated biphenyls (PCBs 180–201) were more abundant in thread herrings and mullets than in Galapagos sea lion pups. This indicates the possible role of biotransformation, reduced uptake of PCBs, or a natural placental barrier for heavier PCBs in sea lions. Lower chlorinated PCB congeners, ranging from PCB 43/44 to PCB 118 (Tetra to Penta- chlorinated biphenyls), make up an important contribution (≈ 37% ± 7.25%) to the total PCB concentrations suggesting a lighter PCB signature ("equatorial fingerprint") in the Galapagos sea lion, mullet and thread herring compared to that observed in many arctic

**\***

**\***


Assessing Biomagnification and Trophic Transport of Persistent Organic Pollutants in the Food Chain of the Galapagos Sea Lion (*Zalophus wollebaeki*): Conservation and Management Implications 91

**Galapagos sea lion**

**Mullet**

**Thread herring**

**Figure 3.** Composition of PCB congeners in Galapagos sea lion pups (a), mullet (b) and thread herring

(c). Error bars are standard errors.

**% of PCBs**

**c**

**% of PCBs**

**b**

**% of PCBs**

**a**

\*Homocedastic: Welch's analysis of variances not used; \*\*Heteroscedastic: Welch's analysis of variances used; ND = non-detectable concentration

**Table 1.** POP concentrations (*μ*g/kg lipid) in Galapagos sea lion, thread herring and mullet sampled in 2008. Lipid contents are arithmetic mean ± standard deviations (SD). Concentrations are mean ± standard error (SE), and the range is indicated between brackets. Different letters (i.e. A, B, and C) indicate significant differences among sea lion pups and fish species (ANOVA and multi-comparisons Tukey-Kramer (HSD) post-hoc test)

**PCB** 

non-detectable concentration

Tukey-Kramer (HSD) post-hoc test)

**PCB-99** 11.0 ± 2.07 **A** 8.30 ± 2.70 **A** 0.570 ± 0.073 **B** 2.62 ± 2.14 **B** <0.05\*\*

**PCB-101** 8.70 ± 1.38 **A** 4.30 ±1.38 **A** 0.630 ± 0.186 **B** 3.35 ± 2.70 **B** <0.05\*\*

**PCB-105** 2.05 ± 0.630 **A** 1.30 ± 0.445 **A** 0.205 ± 0.070 **B** 0.760 ± 0.600 **B** <0.05\*\* (0.715–7.40) (0.140–4.10) (0.062–0.374) (0.020–3.70) **PCB-118** 14.0 ± 3.50 **A** 9.70 ± 3.40 **A** 1.00 ± 0.170 **B** 3.80 ± 3.00 **B** <0.05\*\*

**PCB 128** 2.50 ± 0.750 **A** 1.60 ± 0.570 **A** 0.180 ±0.060 **B** 0.560 ± 0.450 **B** <0.05\*\* (0.740–8.76) (0.201–5.25) (0.071–0.350) (0.015–2.80)

**138/163/164** 24.0 ± 6.70 **A** 15.50 ± 5.60 **A** 1.30 ± 0.360 **B** 3.30 ± 2.60 **<sup>B</sup>** <0.05\*

**PCB 146** 6.00 ± 1.40 **A** 2.80 ± 1.10 **A**,**B** 0.40 ± 0.078**B**,**C** 0.600 ± 0.460 **C** <0.05\*\*

**PCB 153** 35.0 ± 8.90 **A** 25.0 ± 9.80 **A** 1.60 ± 0.580 **B** 3.80 ± 3.00 **B** <0.05\*

**PCB-156** 0.610 ± 0.137 **A** 0.40 ± 0.110 **A** 0.17 ± 0.035**A**,**B** 0.400 ± 0.320 **B** <0.05\*\* (0.170–1.60) (0.090–1.07) (0.075–0.240) (0.012–1.96) **PCB-174** 0.680 ± 0.110 **A** 0.420 ± 0.096 **A** 0.090 ± 0.050 **B** 0.370 ± 0.300 **B** <0.05\*\* (0.140–1.30) (0.100–0.860) (0.025–0.230) (0.014–1.80) **PCB 180** 16.0 ± 4.24 **A** 12.0 ± 4.40 **A** 1.66 ± 0.420 **B** 1.90 ± 1.50 **B** <0.05\*

(4.99–27.0) (1.30–23.0) (0.390–0.740) (0.090–13.0)

(4.36–18.3) (1.79– 16.4) (0.115–0.980) (0.090–17.0)

(5.70–43.0) (1.26–32.0) (0.710–1.46) (0.118–19.0)

(7.80–80.0) (2.080–50.0) (0.690–2.20) (0.150–16.0)

(2.10–16.0) (0.620–11.5) (0.210–0.570) (0.030–3.00)

(11.3–99.3) (2.60–95.4) (0.601–3.10) (0.180–19.0)

(3.90–44.0) (1.00–44.0) (0.600–2.60) (0.130–9.10)

(0.965–9.50) (0.470–4.55) (0.230–0.840) (0.080–4.32)

(0.140–5.60) (0.050–2.00) (0.060–0.240) (0.030–1.80) **PCB 202** 0.355 ± 0.180 **A** 0.160 ± 0.050 **A** 0.070 ±0.020 **A** 0.120 ± 0.090 **A** >0.05\* (0.022–1.90) (0.008–0.470) 0.033–0.126 0.010–0.600 **∑PCBs** 136 ± 32 **A** 91.0 ± 30.0 **A** 9.35 ± 1.90 **B** 28.0 ± 22.0 **B** <0.05\*\*

**PCB-183** 2.20 ± 0.669 **A** 1.40 ± 0.536 **A** 0.215 ± 0.072 **B** 0.440 ± 0.350 **B** <0.05\* (0.516–7.45) (0.170–5.26) 0.008–0.330 0.030–2.20 **PCB 187** 3.40 ± 0.812 **A** 1.45 ± 0.43 **A,B** 0.620 ± 0.130 **B** 0.930 ± 0.680 **B** <0.05\*

**PCB 201** 1.20 ± 0.515 **A** 0.60 ± 0.20 **A,B** 0.140 ± 0.04**A**,**B** 0.370 ± 0.280 **B** <0.05\*

\*Homocedastic: Welch's analysis of variances not used; \*\*Heteroscedastic: Welch's analysis of variances used; ND =

**Table 1.** POP concentrations (*μ*g/kg lipid) in Galapagos sea lion, thread herring and mullet sampled in 2008. Lipid contents are arithmetic mean ± standard deviations (SD). Concentrations are mean ± standard error (SE), and the range is indicated between brackets. Different letters (i.e. A, B, and C) indicate significant differences among sea lion pups and fish species (ANOVA and multi-comparisons

(50.2–384) (16.0–282) (5.40–14.0) (1.20–138)

**Figure 3.** Composition of PCB congeners in Galapagos sea lion pups (a), mullet (b) and thread herring (c). Error bars are standard errors.
